SKIP Regulates ABA Signaling through Alternative Splicing in Arabidopsis

Zhang, Wei; WEI, Jialong; Gao, Zhaoxu; Guan, Jianing; Cui, Zhibo; Wang, Xiaoxue

doi:10.1093/pcp/pcac014

Cited by 15 publications

(11 citation statements)

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“…S4 A). SKIP regulates core ABA signaling genes, including ABF s and PP2C s, which improves Arabidopsis abiotic stress tolerance [ 37 ]. The observed cold-induced downregulation of SKIP17 may be responsible for the reduced cold sensitivity of Dendrobium spp.…”

Section: Discussionmentioning

confidence: 99%

Physiological and transcriptomic comparisons shed light on the cold stress response mechanisms of Dendrobium spp

Li,

Lu,

et al. 2024

BMC Plant Biol

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Background Dendrobium spp. comprise a group of tropical orchids with ornamental and medicinal value. Dendrobium spp. are sensitive to low temperature, and the underlying cold response regulatory mechanisms in this group are unclear. To understand how these plants respond to cold stress, we compared the transcriptomic responses of the cold-tolerant cultivar ‘Hongxing’ (HX) and the cold-sensitive cultivar ‘Sonia Hiasakul’ (SH) to cold stress. Results Chemometric results showed that the physiological response of SH in the later stages of cold stress is similar to that of HX throughout the cold treatment. Orthogonal partial least squares discriminant analysis (OPLS–DA) revealed that soluble protein content and peroxidase activity are key physiological parameters for assessing the cold tolerance of these two Dendrobium spp. cultivars. Additionally, weighted gene co-expression network analysis (WGCNA) results showed that many cold response genes and metabolic pathways significantly associated with the physiological indices were enriched in the 12 detected modules. The Kyoto Encyclopedia of Genes and Genomes (KEGG) and gene ontology (GO) enrichment analyses of the 105 hub genes showed that Dendrobium spp. adapt to cold stress by regulating signal transduction, phytohormones, transcription factors, protein translation and modification, functional proteins, biosynthesis and metabolism, cell structure, light, and the circadian clock. Hub genes of the cold stress response network included the remorin gene pp34, the abscisic acid signaling pathway-related genes PROTEIN PHOSPATASE 2 C (PP2C), SNF1-RELATED PROTEIN KINASE 2 (SnRK2), ABRE-BINDING FACTOR 1 (ABF1) and SKI-INTERACTING PROTEIN 17 (SKIP17), the Ca2+ signaling-related GTP diphosphokinase gene CRSH1, the carbohydrate-related gene STARCH SYNTHASE 2 (SS2), the cell wall biosynthesis gene CINNAMYL ALCOHOL DEHYDROGENASE (CAD7), and the endocytosis-related gene VACUOLAR PROTEIN SORTING-ASSOCIATED PROTEIN 52 A (VPS52A). Conclusions The cold-responsive genes and metabolic pathways of Dendrobium spp. revealed in this study provide important insight to enable the genetic enhancement of cold tolerance in Dendrobium spp., and to facilitate cold tolerance breeding in related plants.

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Section: Discussionmentioning

confidence: 99%

Physiological and transcriptomic comparisons shed light on the cold stress response mechanisms of Dendrobium spp

Li,

Lu,

et al. 2024

BMC Plant Biol

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“…Our results are also in agreement with multiple pieces of evidence associating different components of the spliceosome with redundant and complex regulation of splicing under abiotic stress. The Sm core protein SmEb is induced by ABA treatment, and also modulates the AS of HAB1 similar to the SKIP splicing factor (Huertas et al, 2019; Hong et al 2021; Zhang et al 2022). In addition, an analysis of thousands of public RNA-seq libraries selected PRMT5 and SKIP as the main regulators of introns present in nuclear-unspliced chromatin-bound polyadenylated transcripts, called post-transcriptionally spliced introns (pts) (Jia et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Antagonistic effects of arginine methylation of LSM4 on alternative splicing during plant stress responses

Agrofoglio,

Iglesias,

Perez-Santángelo

et al. 2023

Preprint

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Arabidopsis PROTEIN ARGININE METHYLTRANSFERASE 5 (PRMT5) post-translationally modifies RNA-binding proteins by arginine (R) methylation. The impact of this modification on the regulation of RNA processing is largely unknown. Here we use LSM4, a component of the spliceosome, as a paradigm to study the impact of R-methylation on its function in RNA processing. We identify in vivo targets of LSM4 and show that LSM4 regulates alternative splicing of a suite of them. Furthermore, LSM4 affects mRNA levels of some of the targets, showing for the first time its role in both AS and steady-state abundance. Thelsm4andprmt5mutants show a considerable overlap of genes with altered splicing patterns, suggesting that these might be regulated by PRMT5-dependent LSM4 methylation. Wild-type LSM4 and an unmethylable version complement thelsm4-1growth and circadian rhythms defects, suggesting that methylation is not critical for growth in normal environments. However, LSM4 methylation increases with ABA and is necessary for plants to respond properly to salt stress. In contrast, LSM4 methylation is reduced by bacterial infection, and plants expressing unmethylable LSM4 are more resistant than plants expressing wild-type LSM4. This tolerance correlates with decreased intron retention of immune-response genes upon infection, augmenting the functional isoform. Taken together, this provides the first direct evidence that R methylation adjusts LSM4 function on pre-mRNA splicing in an antagonistic manner in response to biotic and abiotic stress.HighlightPlease provide a statement that, in fewer than 30 words, highlights the novelty of the paper for the non-expert.Arginine methylation of the LSM4 spliceosome component by PROTEIN ARGININE METHYLTRANSFERASE 5 fine-tunes alternative splicing of a set of stress-related genes to antagonistically control biotic and abiotic responses in Arabidopsis.

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“…The role of HAB1.1 is to promote germination, whereas the role of HAB1.2 is to inhibit it ( Wang et al., 2015 ). Studies with Arabidopsis mutants in the genes that encode the splicing factors RNA binding motif protein (RMB25), small nuclear ribonucleoprotein E (SmEb), SNW/Ski-interacting protein (SKIP), and ACINUS revealed their involvement in the regulation of AS HAB1 ( Cheng et al., 2017 ; Bi et al., 2021 ; Hong et al., 2021 ; Zhang et al., 2022b ) ( Figure 3 ). Mutants in these genes are hypersensitive to ABA during seed germination and show an altered expression pattern of HAB1.1 and HAB1.2 isoforms.…”

Section: The Alternative Splicing Modulates Aba Signaling Components ...mentioning

confidence: 99%

“…This influences the ABI5-ABI3 complex formation efficiency, suggesting different roles of those two ABI5 isoforms in regulating the ABA signaling under changing environmental conditions (Zou et al, 2007). As previously mentioned, two alternatively spliced isoforms of ABI5 have also been identified in Arabidopsis in recent studies of the skip-1 mutant in response to ABA during seed germination (Zhang et al, 2022b).…”

mentioning

confidence: 91%

“…Studies using smeb-1 Sugliani et al, 2010;Punzo et al, 2020McKibbin et al, 2002Wilkinson et al, 2005;Fan et al, 2007;Gagete et al, 2009;Gao et al, 2013; This confirms that the AS HAB1.1 variant is the functional HAB1 isoform regulating seed germination. Other studies using a mutant in the SKIP gene showed that apart from regulating HAB1 splicing, it also directly regulates AS of other genes of the core ABA signaling pathway, such as PYRABACTIN RESISTANCE-LIKE 7 (PYL7), PYRABACTIN RESISTANCE-LIKE 8 (PYL8), ABA INSENSITIVE 1 (ABI1), and ABI5 (Zhang et al, 2022b). In response to ABA in the skip-1 mutant, the number of transcripts of functional isoforms of positive ABA regulators PYL7, PYL8, PYL10, ABSCISIC ACID RESPONSIVE ELEMENT-BINDING FACTOR 1 (ABF1), ABF2, and ABI5 are reduced.…”

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confidence: 99%

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Alternative splicing in ABA signaling during seed germination

Sybilska

Daszkowska‐Golec²

2023

Front. Plant Sci.

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Seed germination is an essential step in a plant’s life cycle. It is controlled by complex physiological, biochemical, and molecular mechanisms and external factors. Alternative splicing (AS) is a co-transcriptional mechanism that regulates gene expression and produces multiple mRNA variants from a single gene to modulate transcriptome diversity. However, little is known about the effect of AS on the function of generated protein isoforms. The latest reports indicate that alternative splicing (AS), the relevant mechanism controlling gene expression, plays a significant role in abscisic acid (ABA) signaling. In this review, we present the current state of the art about the identified AS regulators and the ABA-related changes in AS during seed germination. We show how they are connected with the ABA signaling and the seed germination process. We also discuss changes in the structure of the generated AS isoforms and their impact on the functionality of the generated proteins. Also, we point out that the advances in sequencing technology allow for a better explanation of the role of AS in gene regulation by more accurate detection of AS events and identification of full-length splicing isoforms.

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SKIP Regulates ABA Signaling through Alternative Splicing in Arabidopsis

Cited by 15 publications

References 58 publications

Physiological and transcriptomic comparisons shed light on the cold stress response mechanisms of Dendrobium spp

Physiological and transcriptomic comparisons shed light on the cold stress response mechanisms of Dendrobium spp

Antagonistic effects of arginine methylation of LSM4 on alternative splicing during plant stress responses

Alternative splicing in ABA signaling during seed germination

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